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Many researchers have hailed transgenic insecticidal

Transgenic Insecticidal Corn: Beyond Insecticidal Toxicity to Ecological Complexity JOHN J. OBRYCKI, JOHN E. LOSEY, ORLEY R. TAYLOR, AND LAURA C. H. JESSE Many researchers have hailed transgenic insecticidal
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Transgenic Insecticidal Corn: Beyond Insecticidal Toxicity to Ecological Complexity JOHN J. OBRYCKI, JOHN E. LOSEY, ORLEY R. TAYLOR, AND LAURA C. H. JESSE Many researchers have hailed transgenic insecticidal crops plants modified to produce insecticidal proteins derived from genes of the bacterium Bacillus thuringiensis (Bt) as the most important technological advancement in insect pest management since the development of synthetic insecticides (Vaeck et al. 1987, Koziel et al. 1993, Perlak et al. 1990, 1993). At least 18 transgenic insecticidal crops have been field-tested in the United States, and three (corn, cotton, and potato) have been widely planted (Andow and Hutchison 1998, Federici 1998, Gould 1998, USDA 1999). But as the commercial availability of these crops has grown, so too has controversy over how to assess and manage the risks posed by this method of pest control. The widespread planting of millions of hectares of transgenic crops with high levels of insecticidal proteins raises concerns that pest populations might develop resistance to Bt toxins and that food webs might be disrupted (Gould 1998, McGaughey et al. 1998, Marvier 2001). Indeed, the US Environmental Protection Agency (EPA) requires industry to maintain populations of susceptible (nonresistant) insect pests to slow development of resistant populations. Nor are concerns limited to the United States: Anxiety over the safety of food and products derived from transgenic crops have created tensions among international trading partners (Balter 1997, Butler and Reichhardt 1999, Masood 1999). In this article we focus on transgenic insecticidal corn (Bt corn) developed for selected lepidopteran species that feed on above-ground portions of the corn plant. Over 2.8 million hectares of Bt corn were planted in the United States in 1998, limited only by seed availability (Andow and Hutchison 1998); an estimated 9.7 million hectares of Bt corn were planted in Thus, although acreage declined to approximately 6.2 million hectares in 2000, Bt corn is now the most common management tactic for the European corn borer, Ostrinia nubilalis, throughout the corn-growing regions of the United States. The potential benefits of transgenic insecticidal corn include savings in resources devoted to scouting for pest insects, reduced applications of broad-spectrum insecticides, increased or protected yields due to season-long control of O. nubilalis ANALYSIS OF TRANSGENIC INSECTICIDAL CORN DEVELOPED FOR LEPIDOPTERAN PESTS REVEALS THAT THE POTENTIAL BEN- EFITS OF CROP GENETIC ENGINEERING FOR INSECT PEST MANAGEMENT MAY NOT OUTWEIGH THE POTENTIAL ECOLOGICAL AND ECONOMIC RISKS (Rice and Pilcher 1998), protection of stored corn from lepidopteran insect pests (Giles et al. 2000), and lower mycotoxin levels due to a reduction in fungal plant pathogens associated with O. nubilalis feeding (Munkvold et al. 1997, 1999). Balanced against these potential benefits are possible drawbacks. Such disadvantages of genetically modified crops can, in general, be grouped into three categories: (1) selection for resistance among populations of the target pest, (2) exchange of genetic material between the transgenic crop and related plant species, and (3) Bt crops impact on nontarget species. The potential for O. nubilalis to develop resistance to toxins in Bt corn has been discussed in several publications (Gould 1998, McGaughey et al. 1998, Huang et al. 1999). Although the transfer of genetic material between Bt corn and its wild relatives can be a concern (Snow and Palma 1997, Bergelson John J. Obrycki ( is a professor in the Department of Entomology and chair of the Ecology and Evolutionary Biology program, Iowa State University, Ames, IA 50011; Laura C. H. Jesse, an EPA STAR (Science to Achieve Results) Fellow, also works in the Department of Entomology at Iowa State. John E. Losey is an assistant professor in the Department of Entomology at Cornell University, Ithaca, NY Orley R. Taylor is a professor in the Department of Entomology and in the Department of Ecology and Evolutionary Biology at the University of Kansas, Lawrence, KS American Institute of Biological Sciences. May 2001 / Vol. 51 No. 5 BioScience 353 a. b. Figure 1. (a) Assessment of the risks from Bt corn based solely on toxicological studies that examine direct effects of Bt toxins on potential nontarget organisms. (b) A broader ecological assessment of nontarget effects of Bt corn based on the dispersal of transgenic corn pollen and potential trophic-level effects on natural enemies. et al. 1998, Traynor and Westwood 1999), the potential for that transfer is limited to Mexico and Central America, where the wild species are located (Galinat 1988). The impact of Bt corn on nontarget species We focus in this article on the potential negative effects of Bt corn on nontarget species specifically, the impact on arthropods and microorganisms associated with corn. Recent studies documenting negative impacts indicate that nontarget effects may be subtle and complex, and thus may be overlooked in the risk assessment conducted during the registration process for governmental approval of this transgenic crop (Figure 1a). Indeed, we examined the Web sites of EPA and APHIS (Animal Plant Health Inspection Service, US Department of Agriculture) and found no indication that potential ecological interactions had been analyzed during the registration process for transgenic corn. In this article we discuss those ecological effects on several trophic levels within and outside cornfields. Among species that were not explicitly considered in the registration process but that may be adversely affected by Bt corn pollen is the monarch butterfly (Danaus plexippus), which we use as a case study in this article. Predators and parasitoids Because research has shown that microbial insecticide formulations of Bt have some negative effects on natural enemy species (Croft 1990, Laird et al. 1990, Glare and O Callaghan 2000), it is important to determine the impact of Bt corn on populations of insect predators and parasitoids in the corn ecosystem. Numerous insect species attack the European corn borer in North America, including several predatory species with relatively broad host ranges and insect parasitoids that are specific to O. nubilalis (Steffey et al. 1999). Transgenic corn affects natural enemies in several ways: The enemy species may feed directly on corn tissues (e.g., pollen) or on hosts that have fed on corn, or host populations may be reduced (Hoy et al. 1998). Data submitted for governmental registration of transgenic crops appear to focus primarily on direct feeding on corn tissues (USEPA 1999). Because several species of insects that attack the corn borer also feed on corn pollen, researchers have examined the effects of corn pollen on these species (Table 1). Direct consumption of transgenic corn pollen by immature stages of three predatory species commonly found in cornfields did not affect development or survival (Pilcher et al. 1997a). The mortality rate of nymphal stages of the predator Orius majusculus was much the same when fed a thrips species reared on Bt corn as when the thrips were fed on non-bt corn (Zwahlen et al. 2000). However, increased mortality of lacewing (Chrysoperla carnea) larvae was observed when the larvae fed on an artificial diet containing Bt toxin or preyed on corn borers or other lepidopteran larvae that had fed on transgenic corn (Hilbeck et al. 1998a, 1998b, 1999). Indirect negative effects on predators have not been documented in the field; sampling from transgenic cornfields has not shown declines in predator abundance (Orr and Landis 1997, Pilcher 1999). In one field study, higher numbers of predators were observed in Bt cornfields (Table 1). The potential trophic-level effects of Bt corn on vertebrate predators also need to be considered in an ecological assessment of this biotechnology (Figure 1b), because bats and birds are known to prey on larvae and adults of several lepidopteran corn pests. Feeding Bt toxin directly to bobwhite quail for 14 days produced no evident effect on the quail (USEPA 1999). We are not aware of any studies that have considered the indirect effects on bird populations resulting from declines in O. nubilalis densities after use of transgenic corn.however, if Lepidoptera and their predators and parasitoids are significantly reduced in Bt cornfields and adjacent margins, we might expect the insect prey available for birds, rodents, and amphibians to decrease (see Watkinson et al for a simulation of the potential effects of herbicide-tolerant crops on seed-eating birds). When Bt sprays were purposely used to reduce caterpillar abundance in a forest, fewer blackthroated blue warbler nests were observed in sprayed areas (Rodenhouse and Holmes 1992). In one of the four years in 354 BioScience May 2001 / Vol. 51 No. 5 Table 1. Interactions between natural enemies and transgenic insecticidal corn (Bt corn). Location of Effect study ( = negative; Species and (L = Lab; + = positive; Aspect of natural insect predator F = Field) 0 = no effect) enemy showing an effect Reference Neuroptera: Chrysopidae Chrysoperla carnea F 0 Number of adults Pilcher 1999 L 0 Larval development and survival Pilcher et al. 1997a on transgenic pollen L Larval survival on Hilbeck et al transgenic pollen or prey 1998a, 1988b, 1999 exposed to Bt toxins L 0 Larval development and survival Lozzia et al on aphid prey reared on Bt corn Coleoptera: Coccinelllidae Coleomegilla maculata F 0 Number of adults and larvae Orr and Landis 1997 F 0,+ Greater number of adults Pilcher 1999 L 0 Larval development and survival Pilcher et al. 1997a on transgenic pollen Cycloneda munda F 0 Number of adults Pilcher 1999 Hippodamia convergens F 0 Number of adults Pilcher 1999 Hemiptera: Anthocoridae Orius insidiosus F 0 Numbers of adults and nymphs Orr and Landis 1997 F,+ Number of adults Pilcher 1999 L 0 Nymphal survival and development Pilcher et al. 1997a on transgenic pollen Orius majusculus L 0 Nymphal survival and development Zwahlen et al on thrips prey reared on Bt corn Insect Parasitoids Hymenoptera: Braconidae Macrocentris cingulum F 30% 60% reduction in adults Pilcher 1999 (formerly M. grandii) which observations were made, the lack of caterpillar prey led to a reduction in nesting, which is turn lowered breeding activity below that needed to balance annual mortality. In a two-year field study, Pilcher (1999) found abundance of the parasitoid species Macrocentris cingulum (formerly Macrocentris grandii), which is specific to corn borer larvae, to be lower in Bt cornfields in Iowa than in non-bt fields (Table 1), as might be expected because of significant reductions in larval hosts in Bt corn. We predict that the abundance of a second parasitoid species, Erioborus terebrans,will also decline in transgenic fields because of the lack of corn borer hosts, even though findings from one field study indicated that transgenic corn had no effect on E. terebrans parasitism (Orr and Landis 1997). In this field study relatively small nontransgenic plots were planted within transgenic plots, and O. nubilalis larval hosts were parasitized on the nontransgenic plants. It is possible that Bt corn will show an effect on E. terebrans parasitism only in a field study conducted on a larger scale. Long-term field studies are needed to determine whether the widespread planting of transgenic corn creates an ecological desert with relatively few hosts for natural enemies. in transgenic fields F 0 Parasitism of larval hosts on Orr and Landis 1997 nontransgenic plants within transgenic plots Hymenoptera: Ichneumonidae Erioborus terebrans F 0 Parasitism of larval hosts on Orr and Landis 1997 nontransgenic plants within transgenic plots This type of ecological pattern has been observed following the overuse of insecticides or regional planting of highly resistant crop varieties (Gould 1991, 1998). The interactions among natural enemy and pest populations will probably occur within a mosaic of transgenic and nontransgenic cornfields because of the regulatory requirement that susceptible corn borer populations be maintained in nontransgenic corn refugia. If corn borer densities are significantly suppressed by the use of transgenic corn, it might follow that significant reductions in natural enemy densities will occur also, which could influence the rate of development of resistant pest populations (Gould et al. 1991, Johnson et al. 1997). Natural enemies now account for a high level of mortality of the corn borer (Phoofolo and Obrycki n.d.). If this level of mortality were lowered and corn borer populations developed resistance, the result could be higher densities of the corn borer. Thus, the negative impact on natural enemies raises the possibility that overuse of transgenic corn could lead to the types of resurgence and secondary-pest outbreaks that are associated with misuse of synthetic broad-spectrum insecticides. May 2001 / Vol. 51 No. 5 BioScience 355 Insect herbivores The foundation for regulation of transgenic Bt crops is based on a history of relatively safe use of Bt sprays (Laird et al. 1990, Miller 1998, Glare and O Callaghan 2000). The rapid breakdown of Bt toxins in the environment reduces the effects on nontarget organisms, although studies of the ecological interactions of Bt insecticide sprays have documented some effects on nontarget organisms. For example, Tyria jacobaeae, a beneficial lepidopteran introduced into North America for biological control of the weed tansy ragwort, has been found in laboratory bioassays to have increased mortality of fourth and fifth instars after feeding on tansy ragwort leaves dipped in Bt (James et al. 1993). Bt sprays can affect nontarget Lepidoptera for up to 30 days after spraying (Johnson et al. 1995), and Bt drift effects have been observed up to 3000 meters from a spray site (Whaley et al. 1998). Furthermore, a reduction in lepidopteran species richness was found 2 years after forest plots were sprayed with Bt (Miller 1990). Many species of Lepidoptera, both target and nontarget, are likely to be directly susceptible to the Bt toxins produced by transgenic corn hybrids. Because herbivores that feed on corn plant tissue within the cornfield are considered target pests, we consider nontarget herbivores to be those species that may contact corn pollen on weedy plant species within fields or on plants outside of fields. The lepidopteran species most likely to be affected by Bt corn pollen can be determined by examining their distribution and phenology (Losey et al. 2001). Plant communities within range of corn pollen dispersal will, to a large degree, determine which herbivore (and therefore natural enemy) species are most likely to be present and subject to the effects of Bt corn pollen. An initial list of nontarget lepidopteran species can be generated by cross-referencing the species of plants likely to be found near corn with the species of Lepidoptera that feed on these and related plant species. Because many plant species in and around cornfields are considered to be weeds, the makeup of these plant communities is fairly well known. Unfortunately, what knowledge is lacking for most of the plants associated with corn is the proportion of their total distribution that is composed of field edges and the species composition of the lepidopteran fauna. Specialist herbivores that feed on plants that grow exclusively near corn would be of particular interest. These herbivore species may be more likely to be affected by Bt corn pollen than are herbivores that feed on plants growing in several habitats in addition to cornfield margins. Once it has been determined which lepidopteran species feed on plants within the shadow of corn pollen, the next step is to determine which subset of those lepidopteran species are feeding in the larval stage during the period that corn pollen is shed. Individual cornfields shed pollen for 8 to 10 days between late June and mid-august (the period varies with corn hybrid and latitude). Thus, to encounter corn pollen, larvae must be feeding during or after this period, while the corn pollen is still on the host plant. Unfortunately, we do not know how long pollen remains on plants adjacent to cornfields or how long the Bt toxin remains active within corn pollen. The final step in predicting which lepidopteran species are likely to be affected is to determine the relative susceptibility of each species to Bt toxins expressed in transgenic corn pollen. Although the toxin in Bt corn is active against several lepidopteran families, variation in susceptibility has been observed (Pilcher et al. 1997b, Williams et al. 1997, 1998, Wraight et al. 2000). It may be possible to link susceptibility and phylogeny to allow prediction of susceptibility of a given lepidopteran species. Integrating distribution, phenology, and susceptibility permits a ranking of the risk to specific lepidopteran species. Species at particularly high risk could then be identified for further testing. Case study: The monarch butterfly The monarch butterfly, Danaus plexippus, is widely distributed in North America, producing up to five generations in the United States and Canada (Brower 1996). Several factors may make the risk to monarch butterflies from Bt corn pollen higher than risks to other nontarget lepidopteran species. Monarchs migrate annually in spring and summer from overwintering sites in Mexico to breeding areas across eastern North America (Brower 1996). Fifty percent of the overwintering adults in Mexico originate from the central United States, the major corn-growing area in North America (Wassenaar and Hobson 1998). The common milkweed, Asclepias syriaca, is a secondary successional plant that frequently occurs in and around the edges of cornfields (Bhowmik 1994, Yenish et al. 1997, Hartzler and Buhler 2000); it is the primary host plant of monarch butterflies in the northern United States and southern Canada (Malcolm et al. 1989), and monarch larvae feed exclusively on milkweed leaves (Malcolm et al. 1993). Monarch females oviposit on milkweeds throughout the summer; the egg laying that gives rise to the fall migratory generation occurs from approximately 20 July to 5 August in the northern half of the corn belt. Corn anthesis, in which pollen is dispersed at least 60 meters by the wind (Raynor et al. 1972), coincides with this time period over large areas of the Midwest. Thus, the monarch, milkweeds, and Bt-corn pollen overlap spatially and temporally in the central United States. A recent study has shown that monarch larvae reared for 96 hours in the laboratory on milkweed leaves dusted with pollen from Bt corn suffered significantly higher mortality (44%) within 96 hours than did larvae reared on leaves dusted with untransformed corn pollen or leaves without pollen (Losey et al. 1999). In addition, larvae that were fed leaves dusted with pollen from Bt corn consumed significantly less foliage per larva and grew significantly slower. In field studies, transgenic corn pollen was naturally deposited on A. syriaca leaves within and adjacent to a transgenic cornfield (Jesse and Obrycki 2001). The levels of pollen deposition were highest on plants within the cornfield and lowest 10 meters from the field edge. 356 BioScience May 2001 / Vol. 51 No. 5 Leaf samples taken from within and at the edge of the cornfield were used to assess mortality of first-instar D. plexippus.within 48 hours, mortality was 20% for those instars exposed to Bt-corn pollen, compared with 0% for those not exposed to Bt-corn pollen and 3% for controls not exposed to any pollen (Jesse and Obrycki 2001 ). Mortality (at 120 hours) of D. plexippus larvae exposed to 135 pollen grains/cm 2 of transgenic pollen for 48 hours ranged from 60% to 70% (Jesse and Obrycki 2001). No sublethal effects were observed in adult D. plexipp
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